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Imaging Science in Dentistry 2016; 46: 17-24

http://dx.doi.org/10.5624/isd.2016.46.1.17

A posteriori registration and subtraction of periapical radiographs for the evaluation of


external apical root resorption after orthodontic treatment
Eliane Maria Kreich1,*, Ana Cludia Chibinski2, Ulisses Coelho3, Letcia Stadler Wambier2,
Rosrio de Arruda Moura Zedebski1, Mari Eli Leonelli de Moraes4, Luiz Cesar de Moraes4
1

Department of Dental Radiology, School of Dentistry, Ponta Grossa State University, Ponta Grossa, Paran, Brazil
Department of Pediatric Dentistry, School of Dentistry, Ponta Grossa State University, Ponta Grossa, Paran, Brazil
3
Department of Orthodontics, School of Dentistry, Ponta Grossa State University, Ponta Grossa, Paran, Brazil
4
Department of Dental Radiology, School of Dentistry, State University of So Paulo, So Jos dos Campos, So Paulo, Brazil
2

Abstract
Purposes: This study employed a posteriori registration and subtraction of radiographic images to quantify the
apical root resorption in maxillary permanent central incisors after orthodontic treatment, and assessed whether the
external apical root resorption (EARR) was related to a range of parameters involved in the treatment.
Materials and Methods: A sample of 79 patients (mean age, 13.52.2 years) with no history of trauma or endo
dontic treatment of the maxillary permanent central incisors was selected. Periapical radiographs taken before and
after orthodontic treatment were digitized and imported to the Regeemy software. Based on an analysis of the posttreatment radiographs, the length of the incisors was measured using Image J software. The mean EARR was
described in pixels and relative root resorption (%). The patients age and gender, tooth extraction, use of elastics,
and treatment duration were evaluated to identify possible correlations with EARR.
Results: The mean EARR observed was 15.4412.1 pixels (5.1% resorption). No differences in the mean EARR
were observed according to patient characteristics (gender, age) or treatment parameters (use of elastics, treatment
duration). The only parameter that influenced the mean EARR of a patient was the need for tooth extraction.
Conclusion: A posteriori registration and subtraction of periapical radiographs was a suitable method to quantify
EARR after orthodontic treatment, and the need for tooth extraction increased the extent of root resorption after
orthodontic treatment. (Imaging Sci Dent 2016; 46: 17-24)
 oot Resorption; Orthodontics; Subtraction Technique; Image Processing, Computer-Assisted; Tooth Extraction
Key words: R

Introduction
The interaction between orthodontic forces and the peri
odontal ligament leads to an inflammatory phenomenon
that induces apical resorption by clastic activity1 without
clinical symptoms. This phenomenon is known as external
apical root resorption (EARR), and it is an undesirable2
and irreversible side effect of orthodontic treatment.
The reported occurrence of EARR is between 48% and
Received October 1, 2015; Revised November 4, 2015; Accepted November 22, 2015
*Correspondence to : Prof. Eliane Maria Kreich
Department of Dental Radiology, School of Dentistry, Ponta Grossa State University,
General Carlos Cavalcanti Avenue, #4748, CEP 84030-900, Ponta Grossa, Paran,
Brazil
Tel) 55-42-99171983, Fax) 55-42-32203102, E-mail) elianekreich@gmail.com

66% according to radiographic studies and more than 90%


based on histologic analyses.3,4 Fortunately, most cases
exhibit resorption of no greater than 1 mm, which does not
impair tooth function. However, higher degrees of root
shortening are observed in approximately 8% of patients
one year after orthodontic treatment.5
Several factors are associated with EARR, including increased treatment duration, direction of tooth movement,
the loading regimen,2 tooth extraction,1 the type of the
tooth and the malocclusion, and patient-related factors including certain systemic conditions, age, and gender.4
The early detection of initial resorptive lesions during
orthodontic treatment is essential for identifying teeth at
risk of severe resorption.6-8 The subsequent interruption

Copyright 2016 by Korean Academy of Oral and Maxillofacial Radiology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0)
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Imaging Science in DentistrypISSN 2233-7822 eISSN 2233-7830

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A posteriori registration and subtraction of periapical radiographs for the evaluation of external apical root resorption after orthodontic treatment

of active treatment can help to reduce adverse outcomes


during later stages of treatment,7 as well as avoiding or
limiting the potential damage to the patient.9
The tools most commonly used to detect EARR are
periapical1,8 and panoramic radiographs.10 This is probably
due to the frequent use of these exams during the stages
of orthodontic treatment11,12 and the good cost-benefit out
comes for the patient. Nevertheless, the visual comparison
of radiographs before and after orthodontic treatment to
measure the EARR is subject to discrepancies in clinical
practice, and this technique is not able to detect minor
changes in sequential images.13,14
Moreover, both radiographic techniques have limitations. Panoramic radiographs show a substantial amount
of magnification and do not allow the clear visualization
of the premaxilla.11 Although they exhibit much less distortion,11 periapical radiographs require a certain degree
of root shortening to have taken place before it is detectable visually on the radiograph.12,14
In order to overcome these problems, cone-beam computed tomography has been suggested as an alternative
to periapical and panoramic radiographs. The scientific
literature indicates that this technique is suitable for the
detection of early EARR.1,12 However, this exam makes
orthodontic treatment more expensive and subjects the
patient to an additional dose of radiation.
As an alternative, this paper proposes a posteriori registration and subtraction of radiographic images and the
use of computerized techniques to quantify the EARR using periapical radiographs. The procedure of a posteriori
registration and subtraction corrects the discrepancies of
the geometric projection and equalizes the density and the
contrast of the radiographic images before and after treatment, enabling the comparison of the two radiographs and
improving the sensitivity and the accuracy of the evaluation, which is performed using specific software.
Although this method has been extensively tested in
vitro in extracted teeth with simulated resorption,5,7,15-19
the use of periapical radiographs from actual orthodontic
treatments,6,20 as proposed in this paper, is not a common
feature of the dental literature on digital subtraction (DSR)
radiography and EARR.
The null hypotheses tested were that a posteriori registration and subtraction of periapical radiographic images
cannot be used to quantify the EARR following orthodontic treatment and that patient-related factors (gender and
age) and treatment-related factors (tooth extraction, use of
intermaxillary elastics, and duration of orthodontic treatment) do not affect the amount of root resorption.

Therefore, the objective of this retrospective study was


to evaluate whether a posteriori registration and subtraction of radiographic images could be used to quantify api
cal root resorption in maxillary permanent central incisors
after orthodontic treatment, as well as to determine whe
ther the EARR was related to the parameters involved in
the treatment.

Materials and Methods


This study was approved by the Ethical Committee
of So Paulo State University (Campus of So Jos dos
Campos) under protocol #041/2009.
Sample selection

A careful analysis of 300 orthodontic clinical records


from patients treated by dentists who attended a postgrad
uate dental education program in orthodontics was performed. The inclusion criteria were: orthodontic treatment
with the standard edgewise technique; no history of trauma, wear, or endodontic treatment in the maxillary central
incisors; complete radiographic exams, including baseline
and final periapical radiographs of the maxillary central
incisors and cephalometric analysis; the absence of synd
romic or skeletal disorders; and complete root formation
in the maxillary central incisors. After this screening, 79
patients were selected. The sample number was above the
calculated required sample size (n = 64; = 0.5; 1 - =
0.9), but all the selected patients were kept in the sample
to compensate for possible losses during the study.
Radiographic analysis: sequence of procedures

Periapical radiographs were taken using the modified


parallel technique and standardized exposure parameters:
Heliodent 70 (Siemens, Erlangen, Germany) X-ray unit,
70 kVp, 7 mA, 0.4 seconds. The radiographs were digital
ized using a scanner with transparency adapter (HP Scanjet G4050, Hewlett-Packard, Palo Alto, CA, USA) with
a resolution of 300 dpi and 8-bit gray scale. The images
were stored as maximum-quality TIFF format files.
All the images were imported into the Regeemy Image
Registration and Mosaicking 0.2.43-RCB software (DPIINPE, So Jos dos Campos, So Paulo, Brazil). This
software provides image registration and subtraction algorithms (i.e., it corrects geometric discrepancies, equalizes the contrast of two sequential radiographs to make
them comparable, and subtracts the analog pixels values
from two sequential images).
The radiographic image obtained at baseline (before or-

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Eliane Maria Kreich et al

A B

A B
Fig. 2. External apical root resorption is evaluated by the measurement of the long axis of the maxillary central incisors at baseline (A,
Image 1) and in the registered image (B, Image 3).

C D

E F
Fig. 1. Illustrative images of the post-processing procedures of
periapical radiographs for the right maxillary central incisor. Periapical radiographs at baseline (A, Image 1) and after orthodontic
treatment (B, Image 2) were digitalized. The same reference
points are tagged in the pre-treatment (C) and post-treatment (D)
radiographs to align the images and to generate the posteriori registration of Image 3(E). The quality of the registered image (E) is
confirmed by the fact that the subtracted image (F) exhibited the
least possible structural noise.

thodontic treatment) was termed Image 1 and used as the


reference image. The radiographic image obtained after
orthodontic treatment was referred to as Image 2.
Reference points (fixed points in both radiographs) were
selected on both images manually (Fig. 1). These reference points served as coordinates for the software to align
and correct the geometry of the second image according
to the reference image (Image 1). Clearly distinguishable

structures were selected as reference points, such as the


cement-enamel junction and the incisal margin of the max
illary central incisors.
This process generated Image 3, which was the retros
pectively corrected form of Image 2. The quality of the
image correction was visually determined using the image
subtraction routine (Image 1-Image 3). The image registration was considered adequate when the structural noise
on the teeth of interest was reduced to the lowest possible
level, as indicated by a minimal or nonexistent discrepancy in the geometrical position between images, which appears as brighter or darker shades of gray in the subtracted radiograph.
Therefore, the corrected image (Image 3) became the
new follow-up radiographic image, since small differences
in projection angles during exposure or contrast/density
during processing were corrected (Fig. 1).
The evaluation of EARR was performed using Image 1
(baseline) and Image 3 (the corrected image) (Fig. 2). The
measurement of the long axis of the central maxillary
incisors was done using the UTHSCSA Image Tool (University of Texas Health Science Center at San Antonio;
http://compdent.uthscsa.edu/dig/itdesc.html). The length
of the tooth was considered to be the distance between
the root apex and the incisal edge at a specific point corresponding to the mean distance between the mesial and
distal angles. The above-described protocol was carried
out separately for the right and left maxillary central incisors.
The complete procedures of a posteriori registration and
subtraction and DSR were completed by one experienced
investigator trained in this methodology. The measurement
of the length of the tooth was repeated three times and the

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A posteriori registration and subtraction of periapical radiographs for the evaluation of external apical root resorption after orthodontic treatment

Table 1. Mean values of the length of the upper central incisors, angle formed by the maxillary incisor long axis and the nasion line (1.NA),
and linear distance between the most anterior point of the maxillary central incisor and the NA line (1-NA) before and after orthodontic
treatment

Pre-orthodontic treatment
Post-orthodontic treatment
Difference
P-value by paired t-test

Length (pixels)

1.NA ()

1-NA (mm)

302.730.2
287.231.6
15.412.1
(5.1%)
p<0.001

23.67.0
22.26.3
1.48.7
(6.0%)
p = 0.152

5.82.4
5.02.2
0.94.0
(15.0%)
p = 0.0207

final result consisted of the mean of the three evaluations.


Intraexaminer agreement was calculated using Cohens
kappa (k = 0.87).
The EARR in the central maxillary incisors was determined by the difference between baseline (Image 1) and
post-treatment (Image 3) tooth lengths. These values were
obtained in pixels. The difference between the values before and after treatment (mean EARR) was obtained and
described in terms of pixels and relative root resorption (%).
Evaluation parameters

In order to identify possible correlations with factors


that are commonly associated with EARR, data regarding
patient characteristics such as gender and age were collected from the clinical records. The features involved in
the orthodontic treatment that were considered for analysis were the need for maxillary first bicuspid extraction,
the use of elastics, and the treatment duration. The measures 1.NA (angle formed by the maxillary incisor long
axis and the nasion line) and 1-NA (linear distance between the most anterior point of the maxillary central
incisor and the NA line) were also obtained, since these
are part of the cephalometric analysis that determines the
dental pattern of the maxillary incisors.

age, 13.52.2 years; range, 10-19 years; 22 males and 57


females). The mean duration of the treatment was 25.8
6.2 months (range, 10-38 months).
The tooth length before and after orthodontic treatment
was 302.930.3 pixels and 287.232.3 pixels for the
right maxillary central incisors; and 302.430.2 pixels
and 287.231.1 pixels for the left maxillary central incisors. No significant differences were observed when the
right and left central incisors were compared (p>0.05),
and all subsequent analyses were therefore made using the
mean of the measurements of the left and right incisors.
The mean EARR observed was 15.412.1 pixels, representing a resorption of 5.1% (Table 1).
The mean length of the maxillary central incisors, as
well as the mean values of the cephalometric measures
1.NA and 1-NA before and after orthodontic treatment are
shown on Table 1. These parameters exhibited significant
decreases after treatment.
No differences in the mean EARR were observed according to gender, age, the use of elastics, or treatment
duration. The only parameter that influenced the patients
mean EARR was the need for tooth extraction as part of
orthodontic treatment (Table 2).

Discussion

Statistical analysis

The obtained data showed a normal distribution (Shapiro-Wilk). Therefore, the comparisons between mean
tooth length, 1.NA, and 1-NA before and after orthodontic
treatment were made using the paired t-test. The Students
t-test was used to compare the parameters of gender, age,
tooth extraction, elastics use, and treatment duration. The
statistical analysis was conducted using SigmaPlot 12.0
(Systat Software Inc, San Jose, CA, USA), with the significance level set at p = 5%.

Results

The final sample was composed of 79 patients (mean

The data obtained in this study allowed to reject the first


hypothesis tested, since a posteriori registration and subtraction of periapical radiographic images performed using specific software was able to quantify the EARR after
orthodontic treatment. The second hypothesis was partially rejected, because the parameter of tooth extraction
influenced the extent of root resorption.
In our sample, all the patients exhibited EARR to some
degree. This finding was expected and has been widely
documented in the literature.1,2,4,6,9,12,17,21-24 The most com
monly affected teeth are the maxillary incisors,3,25-27 which
is why this paper evaluated resorption in this specific type
of tooth.

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Eliane Maria Kreich et al

Table 2. Mean values of external apical root resorption (EARR) and relative root resorption after orthodontic treatment according to different parameters.

Gender
Male (n = 22; 27.9%)
Female (n = 57; 72.2%)
Age (years)
10 to 12 (n = 32; 40.5%)
>12 (n = 47; 59.5%)
Tooth extraction
Yes (n = 37; 46.8%)
No (n = 42; 53.2%)
Usage of elastics
Yes (n = 60; 76.0%)
No (n = 19; 24.1%)
Treatment duration
12 to 24 months (n = 43; 54.4%)
25 months or more (n = 63; 79.8)

Mean EARR (pixels)

Relative root resorption (%)

17.510.4
14.610.8

5.4%
5.0%

13.98.8
16.511.8

4.7%
5.4%

19.013.3
12.36.5

5.1%
4.3%

15.210.7
16.311.0

5.2%
5.3%

14.710.8
16.410.6

5.0%
5.3%

Most previous studies investigating EARR used the


Malmgren scale to evaluate EARR.9,12,28,29 The scale consists of four scores, varying from no resorption to resorption beyond the apical third of the tooth. It is considered
a subjective method, and the analysis of two radiographs
taken at a temporal interval may introduce some bias,
reflecting the instruction, training, and experience of the
examiner.5,13 Additionally, the diagnosis of root resorption
by the comparison of periapical radiographs is only possible after five to six months.5
The use of a posteriori registration and subtraction over
came these drawbacks. The accuracy of the DSR method
has been confirmed by in vitro studies using extracted
tooth.5,7,8,16 A posteriori registration and subtraction of
periapical radiographic images, the accuracy of which was
checked with DSR, has been proven to be a method that
can quantify small changes associated with EARR in vivo;
in our study, it was possible to diagnose early root loss
(as reflected by changes as small as 0.6 pixels), and our
technique corrected for possible changes in tooth position
resulting from orthodontic treatment.26 In daily practice,
this process can be performed easily. However, the standardization of the follow-up periapical radiographs should
be further developed, since the accuracy of a posteriori
registration may have been higher if the vertical and horizontal angulations did not show variations greater than
20 and 10, respectively.5
Our results showed that the length of the maxillary
incisors diminished by a mean of 15.412.1 pixels or
by approximately 5.1%. These values were measured in
pixels and as relative root resorption (%) because these

P-value (Students t-test)

p = 0.14
p = 0.16
p = 0.003
p = 0.35
p = 0.23

measurement units overcome the inherent variation of the


direct measurement of root length,30 and this is probably
the best way to standardize the results, allowing the fairest comparisons between different papers that evaluate
EARR in a quantitative manner.
Higher mean values have been reported when panoramic radiographs were evaluated (19.512.6 pixels),26 as
well as periapical radiographs (mean EARR percentage of
9.77% after 12 months of orthodontic treatment).31 This
may be expected, since the evaluation of EARR using
panoramic radiographs tends to overestimate the amount
of tooth loss by 20% or more when compared to periapical radiography,11,12 and the evaluation using periapical
radiographs without geometric correction may induce
shortening or lengthening of the image, thereby interfering with the diagnosis.8
Orthodontic treatment produces an apical displacement
of the maxillary incisors. It is highly correlated with apical root resorption32 and with consequent changes in the
values of 1.NA and 1-NA. In our study, both cephalometric measures decreased after orthodontic treatment, which
means that the maxillary central incisors experienced inclination and overall movement in the lingual direction.
Significant changes were observed in the 1-NA measures,
and a reduction of 15% was noted in the protrusion of
the maxillary central incisors after orthodontic treatment;
therefore, the final 1-NA mean value was closer to the
reference value of 4 mm.
The other treatment-related factor evaluated was the
need for tooth extraction, which was the only factor that
showed a significant association with the prevalence of

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A posteriori registration and subtraction of periapical radiographs for the evaluation of external apical root resorption after orthodontic treatment

EARR. Patients who underwent extractions showed a


level of relative root resorption that was 1% higher than
observed in the patients who were treated without extrac
tions. This pattern has also been observed by several other studies.1,9,23,25,27,30,31 When tooth extraction is required,
the maxillary incisors move greater distances than any
other tooth,27,32 with substantial apical displacement.28,31
Therefore, the amount of movement is a risk factor for
apical resorption of the maxillary incisors.9,20
The need for tooth extraction and the necessity of greater tooth movement have frequently been associated with
longer treatment duration.9,25 Some authors have associated root resorption with tooth extraction and the duration
of the treatment,9,25,29-31 while others have found no such
correlation.33-35 A systematic review reported that it is
unclear in the literature whether treatment duration is related to root resorption.3
It must be considered that confounding variables, such
as appointment intervals or the lack of patient cooperation, may increase the treatment duration9 without involving long periods of active forces to the teeth.32 This consideration is the most likely explanation of the conflicting
results in the literature.
In our study, the mean duration of the treatment was
25.86.2 months and it showed no relation with EARR.
Severe EARR has been reported after longer treatment
durations (seven years)9 and in a sample that included
adult patients.29 These differences must be taken into account when comparing our results with those previously
reported in the literature.
The use of elastics has been associated with severe root
resorption when used for more than six months.36 Otherwise, reports have indicated that the use of elastics had no
significant effect on root resorption.35,37 The same results
were obtained in our study. The use of elastics for treatment finishing is common. This practice is patient-dependent and can influence the treatment duration, which may
partially explain the conflicting results in the literature.
The severity of root resorption cannot be fully explained
only by treatment-related factors.29 Therefore, the possi
ble association of gender and age with resorption was
evaluated. These factors were selected because they are
considered potential co-factors of EARR, and clinical trials match samples by these parameters in order to minimize bias.28-30,38 Nonetheless, in our study, EARR was not
influenced by gender or age.
Although a recent paper showed a trend for female patients to exhibit 3% less resorption than male patients,30
other reports have found that male patients have a higher

rate of EARR,35 but most studies have reported that gender had no influence at all on EARR.6,9,25,26,38-40
Regarding to the age criterion, it is often stated that
adults experience more root resorption than teenagers undergoing orthodontic treatment.3,39 This may be related to
the creation of more hyalinized areas, longer hyalinization
duration, and slower healing patterns in adults.31,35 Contrastingly, a systematic review has affirmed that chronological age is not a primary indicator of root resorption,3
but the degree of root formation may be.3,9,41
In our study, the patients age varied between 10 and 19
years. Since complete root formation was an inclusion
criterion for our sample, all patients had completed root
formation. Our upper limit confined the sample to teenage patients. Therefore, the absence of a statistically significant age difference in our sample was expected and
agrees with the observations of maxillary incisors made
by other researchers.25,26,39,42 Nonetheless, it is important
to point out that the criteria of gender and age may not
be reliable predictors of root shortening after orthodontic
treatment.
The multifactorial etiology of EARR complicates the
establishment of a definitive relation with the several factors that cause resorption. This is also related to the heterogeneity of the study designs. The methodologies used
to measure EARR are not standardized, and variations are
present in the radiographic images used for analysis. In
this regard, our study made the contribution of proposing
a methodology that reduces subjectivity when evaluating
root resorption and facilitates early diagnosis. Regardless,
further research on this topic is needed, especially controlled clinical trials with longer follow-up periods.
It may be concluded that a posteriori registration and
subtraction of periapical radiographs is a suitable method
for quantifying EARR after orthodontic treatment, and
that the need for tooth extraction increased the extent of
root resorption after orthodontic treatment.

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